Available via license: CC BY 4.0
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Journal of Biogeography. 2020;00:1–14.
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1wileyonlinelibrary.com/journal/jbi
Received: 8 July 2019
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Revised: 18 Nove mber 2019
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Accepted: 25 N ovember 2019
DOI : 10.1111/j bi.1 3786
RESEARCH PAPER
Phylogenetic diversity and environment form assembly rules
for Arctic diatom genera—A study on recent and ancient
sedimentary DNA
Kathleen R. Stoof-Leichsenring1 | Luidmila A. Pestryakova2 | Laura S. Epp1 |
Ulrike Herzschuh1,3,4
1Alfred Wegener Ins titute Helmholtz
Centre for Polar an d Marine Resear ch, Pola r
Terrestrial Enviro nment al System s, Potsdam,
Germany
2Depar tment for Geography an d Biolog y,
North-Eastern Fede ral Universit y of
Yakutsk, Yakutsk, Russia
3Instit ute of Envir onment al Scie nce and
Geography, Univer sity of Potsdam, Potsdam,
Germany
4Instit ute of Biochemistry an d Biology,
University of Pot sdam , Potsdam, Ger many
Correspondence
Kathle en R. Sto of-Leichsenring , Alfre d
Wegener Institute Helmholtz Ce ntre for
Polar and Marine Research, Polar Terrestrial
Environmental Systems, Telegrafenberg
A45, 14473 Potsdam, Ge rmany.
Email: kathleen.stoof-leichsenring@awi.de
Present address
Laura S. Epp, Uni versit y of Konstanz,
Limnol ogical Instit ute, Mai naustrasse 252,
78464, Konstanz, Germany
Funding information
Federal Minist ry of Edu catio n and Rese arch,
Grant /Award Number: 5.2711. 2017/4.6;
Russian Foundation for Basic Research,
Grant /Award Number: 18-45-140053;
North-Eastern Federal University
Handling Editor: Jani Heino
Abstract
Aim: This study investigates taxonomic and phylogenetic diversity in diatom genera
to evaluate assembly rules for eukar yotic microbes across the Siberian tree line. We
first analysed how phylogenetic distance relates to taxonomic richness and turnover.
Second, we used relatedness indices to evaluate if environmental filtering or compe-
tition influences the assemblies in space and through time. Third, we used distance-
based ordination to test which environmental variables shape diatom turnover.
Location: Yakutia and Taymyria, Russia: we sampled 78 surface sediments and a sedi-
ment core, extending to 7,000 years before present, to capture the forest–tundra
transition in space and time respectively.
Tax o n: Arctic freshwater diatoms.
Methods: We applied metabarcoding to retrieve diatom diversity from surface and
core sedimentary DNA. The taxonomic assignment binned sequence types (lineages)
into genera and created taxonomic (abundance of lineages within different genera)
and phylogenetic datasets (phylogenetic distances of lineages within different genera).
Results: Contrary to our expectations, we find a unimodal relationship between phy-
logenetic distance and richness in diatom genera. We discern a positive relationship
between phylogenetic distance and taxonomic turnover in spatially and temporally dis-
tributed diatom genera. Furthermore, we reveal positive relatedness indices in diatom
genera across the spatial environmental gradient and predominantly in time slices at
a single location, with very few exceptions assuming effects of competition. Distance-
based ordination of taxonomic and phylogenetic turnover indicates that lake environ-
ment variables, like HCO3
− and water depth, largely explain diatom turnover.
Main conclusion: Phylogenetic and abiotic assembly rules are important in under-
standing the regional assembly of diatom genera across lakes in the Siberian tree
line ecotone. Using a space—time approach we are able to exclude the influence of
geography and elucidate that lake environmental variables primarily shape the as-
semblies. We conclude that some diatom genera have greater capabilities to adapt to
This is an op en access arti cle under the ter ms of the Creat ive Commo ns Attri bution License, which permits use, distribution and reproduc tion in a ny medium,
provide d the original wor k is properly cited.
© 2020 The Authors. Journal of Biogeography published by John Wiley & S ons Ltd
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STOOF-LEICHSENR ING ET aL .
1 | INTRODUCTION
Assembly rules constrain the formation of community composition
out of a pool of available species. Exploring which and how intensely
assembly rules affect species composition helps to understand past,
recent and prospective community composition. Particularly in
times of recent global warming it is important to understand how
community composition will change under human-induced, rapid en-
vironmental change compared to natural environmental variability
(Bellard, Bertelsmeier, Leadley, Thuiller, & Courchamp, 2012; Davey
& Blax ter, 2010; Thakur et al., 2017). In environmentally sensitive
Arctic areas, the magnitude of biotic change and its consequences
on ecosystem services (Frainer et al., 2017; Vincent et al., 2012) re-
quire special attention. Globally, too little awareness has been paid
to the effects of global warming on microbial life (Cavicchioli et al.,
2019; Dutta & Dutta, 2016; Heger et al., 2014), which presents an
urgent need to better understand the rules by which microbial as-
semblies are influenced and sustained. The term ‘assembly rules’
was introduced by Diamond in 1975 and different terminologies
have developed since (Götzenberger et al., 2012). In our study we
categorize assembly rules into (a) phylogenetic factors, which are
determined by historical diversification and speciation of taxa, (b)
abiotic (environmental characteristics of the habitat) and biotic (in-
teractions between co-occurring taxa) factors and (c) spatial fac-
tors (geographic distance). These influences of the assembly rules
on taxa composition can be elucidated by looking at the diversity
patterns of communities. Alpha- and beta-diversity measures can be
obtained from taxonomic diversity (based on the number of t axa) as
well as from phylogenetic diversit y (based on the phylogenetic dis-
tance bet ween taxa; Figure 1). Assembly rules in minute life-forms
such as diatoms are less widely explored than in plants (Echeverría-
Londoño et al., 2018; Kraft et al., 2015; Swenson, 2011) or animals
(Arnan, Cerdá, & Retana, 2017) and only a few empirical studies exist
(Bennet t, Cumming, Ginn, & Smol, 2010; Bottin, Soininen, Alard, &
Roseber y, 2016; Rimet et al., 2016; Stoof-Leichsenring et al., 2015).
It is known that diatoms are unicellular eukaryotic minute life-forms
and environmentally highly sensitive (Alverson, 2008). Thus, most
diatom studies find environment to be the major factor determin-
ing diatom communities at different spatial scales by decomposing
the variation in taxonomic community to spatial- versus environ-
mental-related variation (Bennett et al., 2010). Although there is the
expectation that diatoms can freely disperse (Soininen, 2007), other
studies on global diatom distribution find biogeographic (geographic
and evolutionary) factors strongly contribute to diatom community
structure (Vy verman et al., 2007). In general, we have to assume that
similar assembly rules known from plants act on unicellular microbes
such as diatoms (Heino & Soininen, 2005). Because it is known that
morphologically similar diatoms can bear hidden genetic diversity
(Pinseel et al., 2019), adding phylogenetic to taxonomic diversity will
enable us to discern assembly rules in a more robust way (Van den
Wyngaert, Most, Freimann, Ibelings, & Spaak, 2015).
In general, the relative importance of assembly rules to commu-
nity structure can be assessed by null model approaches (deviation
of observed from random patterns). These are used to examine if the
observed co-occurrence of species in a community associate with
the spatial, environmental or biotic similarity of the investigated lo-
cations. To evaluate the relative impact of environment in compar-
ison to the role of geography, it would be advantageous to analyse
diversit y patterns along ecological gradients that provide different
ecological niches over a geographical space and at a fixed place back
in time with different ecological periods at one geographical site.
Under the assumption that evolutionary relatedness is positively
correlated with similar ecological requirements of species, analyses
of phylogenetic diversity allow us to infer the relative importance
of environmental factors and biotic interactions by comparing the
observed diversity with the total diversity in the present assem-
blies (Webb, Ackerly, & Kembel, 2008; Webb, Ackerly, McPeek, &
Donoghue, 2002). A phylogenetic clustering, meaning more closely
relate d tax a in a comm un ity than exp ected by ran dom nul l commu ni -
ties, is probably related to environmental filtering, whereas phyloge-
netically even or over-dispersed communities can be a result of taxa
competition for habitats leading to the exclusion of phylogenetically
similar taxa (Webb et al., 20 02). Because the composition (e.g. spe-
cies richness and phylogenetic diversity) of intrageneric diversity is
generally characterized by species that share ecologically similar re-
quirements due to their close phylogenetic relatedness, the analyses
of generic rather than total community diversity is more suitable to
elucidate the impac t of either competitive exclusion or environmen-
tal filtering (Voskamp, Bake r, Ste ph en s, Vald es , & Will is , 2017; Web b
et al., 2002).
The Siberian tree line presents a huge ecological gradient from
tundra to boreal vegetation with embedded Arctic lake systems and
sediment archives of tree line lakes preserve environmental changes
and diatom communities of the past. Morphological investigations
have attributed Holocene diatom variations to vegetation changes
in the lake catchment s (Herzschuh et al., 2013; Pestr yakova,
Herzschuh, Wetterich, & Ulrich, 2012). A few genetic studies from
the area find that the occurrence of intrageneric diatom lineages is
environmental changes, whereas others will be putatively replaced or lost due to the
displacement of the Arctic tundra biome under recent global warming.
KEYWORDS
ancient sedimentary DNA, Arctic lakes, assembly rules, climate change, diatoms,
environmental filtering, phylogenetic diversity, Siberian tree line
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STOOF-LEI CHSENR ING ET aL .
linked to environmental conditions (i.e. vegetation in the catchment)
rather than geographical constraints (Stoof-Leichsenring et al., 2014,
2015). Because species of a genus are generally composed of eco-
logically similar taxa, addressing diversity within genera will presum-
ably result in stronger competition between taxa of the same genus
than taxa of different genera. Adding a community's phylogenetic
information would then allow us to speculate on the influence of
competition over environment al filtering in intrageneric lineages.
In this case, metabarcoding approaches on sedimentary DNA
using phylogenetically informative marker genes facilitate the anal-
yses of phylogenetic diversit y in natural communities (Nanjappa,
Audic, Romac, Kooistra, & Zingone, 2014), although ancient sedi-
mentar y DNA in particular allows the retrieval of only very short
marker genes and thus limited phylogenetic content (Drummond et
al., 2015; Stoof-Leichsenring et al., 2014). The large subunit of the
Ribulose-1,5-bisphosphate carboxylase/oxygenase (rbcL) has been
used frequently for phylogenetic analyses (Guo, Sui, Zhang, Ren,
& Liu, 2015; Theriot , 2010), but is most powerful in determining
lower taxonomic levels and thus has been used to identify intrage-
nus and intraspecies genetic diversity and diversification (Abarca,
Jahn, Zimmermann, & Enke, 2014; Evans, Wortley, & Mann, 2007;
Hamsher, Evans, Mann, Poulickova, & Saunders, 2011; Kermarrec,
Bouchez, Rimet, & Humbert, 2013). Moreover, short rbcL metabar-
codes have been successfully applied for diatom diversity assess-
ment (Dulias, Stoof-Leichsenring, Pestryakova, & Herzschuh, 2017;
Rimet, Vasselon, A.-Keszte, & Bouchez, 2018). Combining taxo-
nomic with phylogenetic diversity retrieved from sedimentary DNA
archives is a fairly new approach. It offers the opportunity to di-
rectly analyse taxonomic and phylogenetic diversity in space as well
as through time and allows the analysis of community shif ts at one
geographic place under changing environmental conditions. It can
help evaluate the effect of competition between lineages depending
on their phylogenetic relatedness.
This study investigates assembly rules for diatom genera across
the vegetation gradient of the Siberian tree line and via Holocene
time slices of a lake sediment core, which experienced vegetation
changes through time. We combine taxonomic diversity (binning
lineages/sequence types into taxonomically defined genera) and
phylogenetic diversity obtained from a short phylogenetically infor-
mative chloroplast marker specified for metabarcoding using lake
sediments. With our study we aim to evaluate the assembly rules
that structure the community composition of diatoms at the intra-
generic level. First, we investigate how phylogenetic factors (phy-
logenetic distance in diatom genera) af fect taxonomic richness and
turnover in diatom genera. Second, we attempt to discern if abiotic
or biotic factors (environmental filtering or intrageneric competition)
or geography primarily influence the assembly by comparing taxo-
nomic and phylogenetic community signals along a similar ecological
gradient in space as well as through time. Third, we investigate the
extent to which environmental variables and geographic distance
explain taxonomic and phylogenetic turnover.
2 | MATERIAL AND METHODS
2.1 | Material and sampling locations
Sediment and water samples were collected during joint field ex-
peditions of the Alfred Wegner Institute (AWI) and North-Eastern
Federal University of Yakutsk (NEFU) from 78 lakes along a latitu-
dinal transect in the northern lowlands of Yakutia and Taymyria,
Russia. The localities range from the edge of the Arctic tundra over
forest tundra to boreal forest (Figure 2). The lakes investigated were
formed by thermokarst processes and are characterized by their
small size and catchment area and water chemistr y parameters
(Table S1 in Appendix S1). Surface sediments were sampled using a
bottom sampler and subsamples (mainly the first centimetre) were
taken with a sterile spatula and stored in sterile plastic tubes until
further analyses. The sediment core 11-CH-12A was sampled during
an expedition to Chatanga in 2011 and details about sampling and
FIGURE 1 Overview of taxonomic and
phylogenetic diversity metrics used in the
study based on Bray–Curtis dissimilarity
partitioning (phylog. = phylogenetic)
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STOOF-LEICHSENR ING ET aL .
core chronology are described in Stoof-Leichsenring et al. (2015).
Based on pollen analyses, we infer vegetation turnover from the
warmer and forested mid-Holocene period to arctic tundra at the
present day (Klemm, Herzschuh, & Pestryakova, 2016).
2.2 | Genetic assessment of diversity in
diatom genera
Surface sediments were isolated according to the descriptions in
Stoof-Leichsenring et al. (2015), except for the extraction of surface
samples from Taymyr (T Y) and Omoloy (OM) lakes, which were iso-
lated with the same method but in the genetic laboratories at Alfred
Wegener Institute Helmholtz Centre for Polar and Marine Research
in Potsdam. Core sediment samples (11-CH-12A) were handled in
the dedicated ancient DNA laboratory at Alfred Wegener Institute
Helmholtz Centre for Polar and Marine Research in Potsdam, spe-
cially equipped for ancient DNA work. Precise descriptions of the
DNA extraction, PCR amplification of the short rbcL 76bp meta-
barcode and Illumina Next-Generation-Sequencing are given in the
(Appendix S1). For bioinformatic analyses of obtained sequence
reads, we used the OBITools pipeline, which includes a taxonomic
assignment of sequence types with the ecotag algorithm (Boyer et
al., 2016). The complete sequencing data were obtained from two
independent Illumina sequencing runs and were joined after the
OBITools pipeline and further manually filtered (for details see
Appendix S1). After the filtering steps, we kept only sequence types
which were taxonomically identified to diatom genus level and those
genera which occurred in at least 20 of 78 lakes. Similar guidelines
were used for the core data, but genera were kept if they occurred
in 7 of 10 core samples. Then, we split up the entire dataset into
single genus datasets. The final dataset for surface samples of the
lakes comprises 19 different diatom genera, meaning 19 subdata-
sets, whereas the core dataset contains 9 diatom genera resulting
in 9 subdatasets.
2.3 | Taxonomic and phylogenetic diversity metrics
The taxonomic diversity dataset consists of sequence types that
are binned into taxonomically defined genera, whereas the phylo-
genetic diversity datasets are based on the phylogenetic distances
of lineages within the identified genera. We tested the suitability
of the 76bp met abarcode to assess proper phylogenetic distances
within genera by comparing pairwise distances of reference se-
quences covering the shor t (76bp) and three longer rbcL fragments
FIGURE 2 Map of the 78 lake sampling sites across the tree line ecotone in northern Siberia. The map was created with Esri Arc GIS
Version 10.2 and Natural Earth Background Map
07SA07
07SA23
07SA26
07SA31
07SA33
07SA34
09-TK-03
09-TK-04
09-TK-05
09-TK-08
09-TK-09
09-TK-13
09-TK-14
11-CH-02
11-CH-05
11-CH-06/09/10
11-CH-11
11-CH-12/13
/14/15
11-CH-17/19/20
11-CH-18 13-TY- 01
13-TY-02/03/04
/05/06/07
13-TY-08
13-TY-09/1 0/11/12
/13/14/15
13-TY-16
13-TY-17
13-TY-18/1 9/20
/21/22/23/24
13-TY-26/27/28/29
/30/31/32
14-OM-01
14-OM- /03/04/05
/06/07/08/09
14-OM-10
14-OM-11/12/13/14
/15/16/17
14-OM-18/19/20
14-OM-21
150° E
140° E
140° E
130° E
130° E
120° E
120° E
110° E
110° E
100° E
100° E90°E80°E
75°N
75°N
70°N
70°N
65°N
65° N
0100 200km
sites
treeline
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STOOF-LEI CHSENR ING ET aL .
(1398bp, 939bp and 365bp). The 1398bp rbcL fragment have been
successfully used to recover phylogenetic relationships in the genus
Sellaphora (Evans et al., 2007; Vanormelingen, Evans, Chepurnov,
Vyverman, & Mann, 2013) and a slightly shor ter fragment was used
to demonstrate phylogenetic relationships in Aulacoseira (Edgar &
Theriot, 2004). Restricted by the available reference sequences, we
could test intrageneric distances in 4 genera (Sellaphora, Nitzschia,
Navicula and Cyclotella) by comparing the 1398bp and the 76bp rbcL
barcode. We used 11 genera for comparing the 939bp with the 76bp
rbcL barcode and 16 genera in the comparison between the bar-
codes 365bp and 76bp (Table S2 in Appendix S1). The comparison
of pairwise phylogenetic distances between reference sequences
of the short (76bp) and three longer overlapping rbcL fragments re-
vealed significant correlations for all the tested datasets (Table S2),
except datasets Asterionella (76bp vs. 365bp, N = 6) and Melosira
(76bp vs. 939bp, N = 3) showed no significant correlation, which is
most likely due to the low number of available reference sequences
(Table S2 in Appendix S1).
We applied taxonomic and phylogenetic alpha- and beta-di-
versity metrics (Figure 1) on the generic datasets. We calculated
Simpson's diversity (hill 2) as a measure of taxonomic alpha diversity
within genera using the R package ‘vegetarian’ (Charney & Record,
2012) . The Sim ps on di ve rsity gives an esti ma te of th e eff ect ive num-
ber of species (with down-weighting of rare taxa), which, in our study,
is th e nu mb er of diff er ent lineage s wi th in a genus. Prior to th e an al y-
ses of the effective number of taxa in each genus, the dataset s were
rarefied to the minimum number of counts per genus (surface sam-
ples = 1,010, core samples = 391). To obtain the taxonomic beta di-
versity we used R package ‘betapart’ and calculated the Bray–Curtis
dissimilarity to quantify the total taxonomic turnover (bray) for each
genus and th e proportion of repl ac em ent of ta xa (bray.bal ), as well as
abundance gradient components between two sites (Baselga, 2012)
and calculated the overall mean of each metric per genus. Prior to
analyses of t axonomic beta diversity, we rarefied surface and core
data to the minimum sample count (surface samples = 2,899, core
samples = 94,899) and resampled the data to create rarefied data-
sets which were used for the subsequent statistical analyses. For
rarefaction analyses we used the R script (https ://github.com/Stefa
nKrus e/R_Raref action).
For phylogenetic alpha diversity within the genera we calcu-
lated the uncorrected phylogenetic distance (pdist) using Geneious®
11.1.5 and the mean phylogenetic distance (mpd) and mean nearest
taxon distance (mntd) based on abundance weighted and presence/
absence data respectively. The calculation of the phylogenetic dis-
tances between lineages within one genus was conducted using the
R package ‘phangorn’ (Schliep, 2011) by estimating the tree branch
lengths obtained from a maximum likelihood tree (using pml function
with GTR substitution model) derived from phylogenetic distances
(function dist.ml) bet ween the sequence types, which were saved in
fasta format. Phylogenetic distances were then combined with the
abundance data or presence/absence data of the sequence types
within each genus by using the function match.phylo.comm and mpd
and mntd values were calculated with the functions ses.mpd and
ses.mntd respectively. Resulting ses.mpd and ses.mntd values were
converted into net relatedness index (NRI) and nearest taxon index
(NTI), respectively, by multiplying by −1 (using R package ‘picante’;
Kembel et al., 2010). NRI and NTI values in single locations and core
slices were c alculated for the five most abundant genera in surface
and core samples. NRI measures whether the sum of the pairwise
phylogenetic distances among all pairs of taxa (considering differ-
ences in higher t axonomic levels) in the community is more or less
than expected from randomly generated null communities, assum-
ing that positive NRI values indicate environmental clustering, while
negative values indicate even or over-dispersed communities, which
could be attributed to exclusive competition between co-occurring
taxa. NTI measures whether most closely related co-occurring taxa
(mostly within species/genus relationships) in a community are more
or less closely related than expected and follows the same interpre-
tation as NRI. Furthermore, we used the comdist function in the R
package ‘picante’ (Kembel et al., 2010) to calculate phylogenetic beta
diversit y (betaNRI and betaNTI), that is, the phylogenetic distances
between pairs of samples weighted for the abundance of sequence
types and also with presence/absence data. Correlation analyses
and Loess regression were used to evaluate relationships between
the diversity indices and were done in the R package ‘ggplot2’
(Wickham, 2016). Distance-based redundancy analyses (dbRDA)
were run to estimate the influence of geography and environment on
the distance matrix derived from the beta-diversity calculations for
the taxonomic (total turnover and bray) and phylogenetic datasets.
Hence, co-ordinates of the sampling localities were transformed
to rectangular data suitable for ordination methods using principal
co-ordinates of neighbourhood matrix (PCNM), with the function
pcnm. Environmental variables were log(x + 1) transformed using
the log1p fu nct io n and were, togethe r wi th the pr in cipal coord in at es ,
used as constraints for the dbRDA with the dissimilarit y matrices
originating from the taxonomic and phylogenetic datasets using the
function capscale and a subsequent stepwise forward model selec-
tion with the func tion ordistep. The selected constraint s were then
applied to dbRDA and their significance assessed with the function
permutest. The calculations regarding dbRDA were performed using
the R package ‘vegan’ (Oksanen et al., 2019) and all computations
were conducted with RStudio version 1.1.456.
3 | RESULTS
3.1 | Taxonomic and phylogenetic composition
The joined dataset of the two Illumina sequencing runs and subse-
quent filter steps resulted in 19 verified genera each containing be-
tween 6 and 156 sequence types for the 78 lake surface samples and
9 verified genera containing between 5 and 87 sequence types for
the 10 core samples. The sequence t ypes within a genus consist of
intr as pec if ic to int ragen eric se que nc e t yp es, as indic ated by the ir se-
quence match to reference sequences, which varied between 100%
and 90%.
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STOOF-LEICHSENR ING ET aL .
Our results demonstrate strong differences in abundance, rich-
ness, turnover and phylogenetic distance in diatom genera. The
total modern surface dataset consists of 7,534.170 sequence reads,
whereof 95% are assigned to Staurosira, Aulacoseira, Pinnularia,
Melosira, Sellaphora and Stauroneis; the remaining 13 genera repre-
sent <5% of total reads. We identified 986 unique sequence t ypes
and highest richness occurs in Stauroneis, Staurosira, Aulacoseira and
Sellaphora, whereas lowest richness is present in Melosira, Caloneis,
Ellerbeckia and Tabellaria. The taxonomic beta diversity (full replace-
ment of taxa; bray.bal) is highest Nitzschia and Neidium, whereas
Tabellaria and Ellerbeckia show least turnover. In terms of phyloge-
netic distances, Ellerbeckia, Cylotella and Staurosira consist of phylo-
genetically closely related lineages (uncorrected mean pdist varies
between 1.8 and 3.9 nucleotide differences), whereas lineages in
Nitzschia, Stauroneis and Caloneis are most distantly related (uncor-
re cted mea n pdis t varie s between 4. 5 and 12 n u c l e otide d i f f e r e n ces) .
The tot al core dat aset consist of 3,613.450 sequence reads and
234 unique sequence types. About 76% of sequence reads are at-
tributed to Staurosira an d Cyclotella, whereas the richness is highest in
Staurosira, Aulacoseira and Cyclotella. Sellaphora and Stauroneis show
highest turnover, whereas Tabellaria and Asterionella represent gen-
era with low turnover throughout the core slices. Phylogenetically
closest lineages are present in Tabellaria, Cyclotella and Staurosira
(pdist varies between 2.8 and 3.8), whereas Stauroneis, Sellaphora
and Pinnularia compris e most distantl y relat ed lineages. The det ai led
results for all genera are presented in Table S3 in Appendix S1.
3.2 | Phylogenetic distance and taxonomic
richness and turnover in diatom genera
Our re su lt s demon st rate that the var ia ti on in diat om gen era wit h re -
gard to taxonomic richness and turnover is influenced by the mean
phylogenetic distance (mpd) of genera. We show that genera with
more distantly related lineages (high mpd) have high richness (=high
effective number of lineages, hill 2) and greatest turnover (bray.
bal) across the investigated ecotone compared with genera con-
sisting of closely related lineages, which have fewer effective taxa
and show a lower turnover. Two genera (Aulacoseira and Staurosira)
consist of closely related lineages (moderate mpd) with a high num-
ber of effective lineages but a lower turnover across the sampled
area (Figure 3a). This unimodal relationship between the phyloge-
netic distance and richness of diatom genera indicates the effect of
counteracting factors between phylogenetic diversity and richness.
No relationship could be identified between mpd and the effective
number of lineages derived from core samples (Figure 3b). Only
the genus Staurosira is notable as it is characterized by a moderate
mpd but show s a much hi gher ef fe ctive num be r of li neage s than the
other genera.
A clear positive relationship is revealed between the phylogenetic
di s t anc e (mp d ) and th e tu rno ver (bray. bal ) of diat o m gen e ra. Th is me a ns
that genera with closely related sequence types show less turnover
than genera consisting of more distantly related sequence types. This
holds true for either abundance-weighted or presence/absence data
(Table 1, Figure 4). The patterns discerned from the spatial data are
partly mirrored in the core data, although the signal is weaker, prob-
ably due to the smaller number of genera and samples and because
the mean phylogenetic distance is generally lower than from surface
samples, as only a selection of sequence types occurs in the core lo-
cality compared with the larger spatial gradient. However, the positive
relationship between mpd and bray.bal detec ted from surface dat a is
also found for the core data and is most significant when using mpd
values based on presence/absence rather than abundance-weighted
data. Because the positive relationship between mpd and bray.bal is
valid for both surface (spatial) and core (temporal) assemblies of dia-
tom genera—that is, the turnover of taxa through time at a fixed place
FIGURE 3 Relationship between phylogenetic (mean
phylogenetic distance (mpd, abundance.weighted = TRUE) and
taxonomic alpha diversity (Simpson diversity, effective number
of taxa = hill 2) of (a) 19 diatom genera obtained from 78 lake
surface samples and (b) 9 diatom genera from 10 slices of the lake
sediment core 11-CH-12A. For Loess regression (green curve) we
used a 0.5 smoothing factor. Amp, Amphora; Ast, Asterionella; Aul,
Aulacoseira; Cal, Caloneis; Cha, Chaetoceros; Ell, Ellerbeckia; Gom,
Gomphonema; Mel, Melosira; Nav, Navicula; Nei, Neidium; Niz,
Nitzschia; Pin, Pinnularia; Pla, Planothidium; Sel, Sellaphora; Sta,
Staurosira; Stu, Stauroneis; Tab, Tabellaria; Uro, Urosolenia
Amp
Ast
Aul
Cal Cha
Cyc
Ell
Gom
Mel
Nav
Nei
Niz
Pin
Pla
Sel
Sta
Stu
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v
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el
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Uro
Sta
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a
a
A
A
u
l
l
p
Ast
t
t
st
st
ul
l
l
ha
a
a
a
Cyc
c
c
As
As
s
s
s
s
u
Amp
A
p
p
Cal
al
al
Cha
Ch
Ch
Ch
C
Gom
m
m
C
C
Nei
ei
ei
T
ab
b
b
T
T
0.000
0.025
0.050
0.075
246
8
effective number of taxa (hill2)
mean phylogenetic distance
bray.bal
0.2
0.4
0.6
0.8
(a)
Diatom genera in surface lake sediments
R=0.47, p=0.045
Ast
Aul
Cha
Cyc
Pin
Sel
Stu Sta
Tab
A
ul
Cha
a
Pin
i
n
n
el
Stu
u
u
u
Pin
Pin
i
el
el
A
ul
ul
ul
Cha
a
a
a
C
el
el
el
Sta
a
a
T
el
el
ab
a
a
b
T
T
Cyc
c
c
Cyc
c
c
T
T
T
ab
a
a
b
b
T
T
T
T
T
T
−0.1
0.0
0.1
0.2
2.55.0 7.5
mean phylogenetic distance
effective number of taxa (hill2
)
bray.bal
0.2
0.3
0.4
0.5
0.6
(b) Diatom genera in cored lake sediments
R=0.28, p=0.46
|
7
STOOF-LEI CHSENR ING ET aL .
is similar to turnover in space—we presume that geography has less
influence on the regional community assembly than environmental or
biotic assembly rules (Figure 4).
3.3 | Relatedness indices in diatom genera from
surface and core samples
To evaluate the impact of environmental and biotic assembly rules
(e.g. competition) within the five most abundant diatom genera
(Staurosira, Aulacoseira, Pinnularia, Sellaphora and Stauroneis) we
calculated the alpha phylogenetic metrics NRI and NTI for all
surface and core-slice samples (Figure 5). In most of the samples
from the genera datasets we find positive NRI and NTI values
indicating clustering of closely related sequences, although only
some exceed a significant deviation from null communities after
Bonferroni correction (Figure 5). The genera Staurosira, Aulacoseira
and Stauroneis show a strong significant clustering signal in many
investigated localities, whereas for Pinnularia and Sellaphora only
very few samples show this signal. There are no significant nega-
tive NRI or NTI values (after correction), suggesting that few dis-
tantly related lineages co-occur in the samples analysed. Only in
the genera Sellpahora and Stauroneis do NTI values in two sam-
ple sites tend to show over-dispersed communities, supported by
weak p-values.
Most of the genera obtained from core samples indicate a shift
in NRI and NTI values across the different time slices attributed to
vegetation changes over the last 7,0 00 years, but with only a few
samples exceeding the uncorrected/corrected significance thresh-
olds, indicating neither a strong clustering nor a signal of over-dis-
persed communities in the core samples. Exclusively, Staurosira
displays strongly significant positive values indicating a clustering
of closely related sequences in most of the core samples.
3.4 | Taxonomic and phylogenetic turnover
in diatoms
We related total taxonomic and phylogenetic beta diversity of sur-
face samples to environmental variables and geographic distance.
We used distance-based redundancy analysis to test if the ex-
planatory variables (a combination of three lake environment vari-
ables: water depth, pH and hydrogen carbonate) and geographic
components significantly contribute to the variation of taxonomic
and phylogenetic turnover of the five selected genera obtained
from the lake sediment–surface samples (Table 2). Taxonomic and
phylogenetic turnover of the selected genera were always signifi-
can tly co rre lat e d (s ee Mante l tes t re sult s Tab le 2) a nd b oth metr ics
are partly explained by similar variables. However, phylogenetic
turnover in Staurosira is exc lusively ex plain ed by HCO 3
− and water
depth, whereas the other genera are explained by a combination
of different variables. For nearly all analysed datasets, HCO3
− and
water depth are the predominant environmental variables which
contribute to the turnover of selected diatom genera across the
Siberian tree line ecotone, mostly coupled with spatial variables.
Except the genus Aulacoseira is largely explained by geography
and water depth.
4 | DISCUSSION
4.1 | The effect of phylogenetic distance on richness
and turnover in diatom genera
Our study reveals a strong phylogenetic influence on the richness
patterns of diatom genera. We identif y one group of diatom genera
(Asterionella, Amphora, Caloneis, Cyclotella, Chaetoceros, Gomphonema,
Melosira, Neidium, Planothidium, Tabellaria and Urosolenia) character-
ized by low mean phylogenetic distance (mpd) and low richness and
turnover across the Siberian tree line. In contrast, a second group of
genera (Navicula, Nitzschia, Pinnularia, Stauroneis and Sellaphora) is
characterized by high mpd, but with high richness and turnover. A
TABLE 1 Result s of Pearson correlation tests used to analyse
the relationships between diatom's alpha- and beta-diversity
metrics obtained from lake surface and core sediment samples
Diversity metrics
Lakes surface samples
(NGenera = 19)
Lake core samples
(NGenera = 9)
RpRp
Alpha phylogenetic versus taxonomic diversity
mpd.aw versus
hill2
0.466 .045* 0.284 .458
mpd.pa versus
hill2
0.437 . 061•−0.156 .688
mntd.aw versus
hill2
−0.008 .973 −0.402 .284
mntd.pa versus
hill2
0.041 .868 −0.372 .325
Alpha taxonomic versus beta taxonomic diversity
hill2 versus bray.
bal
0.523 .0 21* −0.157 . 687
Alpha phylogenetic versus beta taxonomic diversity
mpd.aw versus
bray.bal
0.662 .002** 0.545 .125
mpd.pa versus
bray.bal
0.638 .003** 0.725 .027*
mntd.aw versus
bray.bal
0.424 .070•0.648 .059•
mntd.pa versus
bray.bal
0.483 .0 36* 0.653 .056•
Note: p values are coded in ***0.001, **0.01, *0.05, •0.1; mpd.aw, mean
phylogenetic distance (method = abundance weighted); mpd.pa, mean
phylogenetic distance (method = presence/absence); mntd.aw, mean
nearest taxon distance (method = abundance weighted); mntd.pa, mean
nearest taxon distance (method = presence/absence); hill2, Simpson
diversity index (effec tive number of ta xa); bray.bal, proportion of taxa
replacement from total taxonomic turnover.
8
|
STOOF-LEICHSENR ING ET aL .
third group is formed by the most abundant genera Staurosira and
Aulacoseira, which are characterized by moderate mpd, but have the
highest richness compared to the other two groups. Our data suggest
that increasing mpd does not lead to a further increase in richness,
which we hypothesize could be a result of ongoing diversification in
the genus Staurosira and Aulacoseira. A similar antagonistic relation-
ship has also been identified in microbes, in which increasing genetic
richness in the absence of an increasing dissimilarity of genotypes
in, for example, homogeneous habitats, has been attributed to re-
duced ecosystem functioning (Jousset, Schmid, Scheu, & Eisenhauer,
2011). The mpd of genera identified in the different time slices of the
core samples do not show a relationship with richness, which could
be a result of the reduced number of genera identified. This may be
caused by technical issues such as degradation of sedimentary DNA
(Parducci et al., 2017) that might bias the retrieved genetic diversity,
or dispersal limitation, which could have restricted the local genetic
richness of diatoms in the past (Verleyen et al., 2009).
The mpd of diatom genera is significantly positively related
to taxonomic turnover (full replacement of taxa) across the tree
line ecotone (vegetation changes from tundra to forest). This re-
lationship is also valid at a single location in one lake, which expe-
rienced climatic and related vegetation changes (as present along
the spatial gradient) through time. We expected this relationship
because genera with more distantly related sequence types are
most probably adapted to different environments and thus would
show greater turnover across the ecological gradient, as has been
reported for microbial diversity (Jousset et al., 2011), whereas
genera consisting of closely related sequence t ypes tend to have
similar requirements and thus show less turnover. This phenom-
enon could also explain the reduced turnover in Staurosira and
Aulacoseira compared to other genera with more distantly related
lineages, assuming that several closely related lineages comple-
ment each other and can persist in different ecological niches
due to their incomplete differentiation across the tree line eco-
tone. Because habitat heterogeneity has been shown to affect
the diversification of diatoms (Nakov, Beaulieu, & Alverson, 2018;
Zorzal-Almeida, Soininen, Bini, & Bicudo, 2017), we assume similar
processes affected Staurosira and Aulacoseira across the ecological
gradient formed by the tree line.
Alternatively, genera with a high turnover along the spatial eco-
logical gradient of the tree line could also result from geographically
structured lineages due to historic events, for example, dispersal
limitation ( Verleyen et al., 2009; Vilmi, Karjalainen, & Heino, 2017).
Because the relationship bet ween mpd and turnover is also present
in a sample series presenting past vegetation changes at one local-
ity, our results support the assumption that mainly environmental
factors shape the turnover in diatom genera across the ecotone,
whereas the impact of geographic factors seems less import ant.
This is also suppor ted by the fact that geographic factor s do not sig-
nificantly explain the variance in, for example, Staurosira across the
tree line. To fully rule out the impact of geography on diatom diver-
sity across the tree line, more time series need to be investigated.
However, in the core samples we identified only a significant cor-
relation between mpd and turnover when using mpd values based
on presence/absence data, which might be related to the degraded
nature of ancient DNA-enhancing PCR bias, for example, and thus
impacting the abundance of sequence types (Krehenwinkel et al.,
2017 ).
4.2 | Environmental filtering shapes diatom
assembly in space and through time
The phylogenetic relatedness of taxa that co-occur in a community
can be used to discern whether the environment or biotic interaction
is responsible for the community assemblage (Webb et al., 2002).
FIGURE 4 Relationship between the mean phylogenetic
distance (method= abundance-weighted) and the t axonomic
turnover (beta diversity) in terms of taxa replacements (bray.bal) of
(a) 19 diatom genera obtained from 78 lake sur face samples and (b)
9 diatom genera from 10 slices of the lake sediment core 11-CH-
12A (method= presence/absence). Size of points indicates the
Simpson diversity (effec tive number of taxa = hill2). Amp–Amphora;
Ast, A sterionella; Aul, Aulacoseira; Cal, Caloneis; Cha, Chaetoceros;
Ell, Ellerbeckia; Gom, Gomphonema; Mel, Melosira; Nav, Navicula;
Nei, Neidium; Niz, Nit zschia; Pin, Pinnularia; Pla, Planothidium; Sel,
Sellaphora; Sta, Staurosira; Stu, Stauroneis; Tab, Tabellaria; Uro,
Urosolenia
Amp
Ast
Aul
Cal
Cha
Cyc
Ell
Gom
Mel
Nav
Nei Niz
Pin
Pla
Sel
Sta
Stu
Tab
Uro
Amp
p
p
Ast
A
Cyc
y
y
c
c
Ast
Ast
t
t
t
t
Gom
o
m
m
N
a
v
v
v
v
v
Niz
z
z
Pin
n
n
n
n
Pla
a
yyc
c
Sel
l
el
Pi
Pi
Sta
S
a
a
Stu
Stu
u
u
0.0
0.3
0.6
0.9
0.00 0.02 0.04 0.06 0.08
mean phylogenetic distance
taxonomic turnover (replacement)
hill2
2
4
6
8
(a)
Diatom genera in surface lake sediments
R=0.66, p=0.002
Ast
Aul
Cha
Cyc
Pin
Sel
Stu
Sta
Tab
Ast
t
t
A
ul
ul
ul
Cha
Cha
C
C
C
a
a
Stu
St
u
u
Sta
Sta
a
a
T
0.25
0.50
0.75
1.00
0.04 0.08 0.12
mean phylogentetic distance
taxonomic turnover (replacement)
hill2
0.2
0.3
0.4
0.5
0.6
(b) Diatom genera in cored lake sediments
R=0.72, p=0.027
|
9
STOOF-LEI CHSENR ING ET aL .
Our study supports that the phylogenetic relatedness of lineages
in five selected diatom genera (using NRI and NTI metrics) primar-
ily indicates a clustering effect defined by the co-occurrence of
closely related lineages in the investigated lake localities. This ef fect
is driven by environmental filtering resulting in the co-occurrence
of lineages due to their similar ecological requirements. This signal
tends to be strongest in the genus Staurosira, which could be a result
of either multiple invasions of minute staurosiroid diatoms into the
FIGURE 5 Scatter plots indicating the NRI (net relatedness index) and NTI (nearest taxon index) values for five selected genera, showing
the standardized effect size of mean phylogenetic diversity (mpd) versus null communities using the method=abundance.weighted, which
includes variation of sequence types abundance in the 78 lake sediment–surface samples across the Siberian tree line and in 10 core
sediment samples (core 11-CH-12A). The background is coloured according to the dominant vegetation type in the vicinity of the sampled
lakes (personal observation and vegetation plot analyses). Sample ages are in calibrated years Before Present (cal yr BP). Vegetation changes
are reconstructed from pollen analyses (Klemm et al., 2016). Significance of relatedness indices is indicated by bubble sizes. p = .0 01
indicates significant deviation of observed mpd versus null communities af ter Bonferroni correction. Gaps indicate no available data. a/b –
Staurosira, c/d – Aulacoseira, e/f – Pinnularia, g/h– Sellaphora, i/j –Stauroneis
−1
0
1
2
3
0
20
40
60
80
surface samples
relatedness indices
type
NRI
NTI
NRI and NTI from surface samples (Staurosira)
even/over-dispersed
communities
phylogenetically clustered
communities
TUNDRAFOREST-TUNDRAFOREST
significance
n.s.
p < 0.05
p = 0.001
−1
0
1
2
relatedness indices
type
NRI
NTI
NRI and NTI from core samples (Staurosira)
significance
n.s.
p < 0.05
p = 0.001
present 600 900 1800 2300 3800 5500 6100 6600 6900
even/over-dispersed
communities
phylogenetically clustered
communities
TUNDRA FOREST-TUNDRA FOREST
(b)
sample age in cal yr BP
−2
−1
0
1
2
3
0
20
40
60
80
surface samples
relatedness indices
type
NRI
NTI
NRI and NTI from surface samples (Aulacoseira)
significance
n.s.
p < 0.05
p = 0.001
TUNDRA FOREST-TUNDRAFOREST
even/over-dispersed
communities
phylogenetically clustered
communities
−2
−1
0
1
relatedness indices
NRI and NTI from core samples (Aulacoseira)
even/over-dispersed
communities
phylogenetically clustered
communities
present 600 900 1800 2300 3800 5500 6100 6600 6900
type
NRI
NTI
significance
n.s.
p < 0.05
p = 0.001
(d)
sample age in cal yr BP
TUNDR
AF
ORESTFOREST-TUNDRA
−1
0
1
2
3
0
20
40
60
80
surface samples
relatedness indices
NRI and NTI from surface samples (Pinnularia)
type
NRI
NTI
significance
n.s.
p < 0.05
p = 0.001
even/over-dispersed
communities
phylogenetically clustered
communities
TUNDRA FOREST-TUNDRA FOREST
(e)
−2
−1
0
1
2
3
relatedness indices
NRI and NTI from core samples (Pinnualria)
TUNDRA FOREST-TUNDRA FOREST
type
NRI
NTI
significance
n.s.
p < 0.05
p = 0.001
even/over-dispersed
communities
phylogenetically clustered
communities
present 600 900 1800 2300 3800 5500 6100 6600 6900
(f)
sample age in cal yr BP
(a)
(c)
10
|
STOOF-LEICHSENR ING ET aL .
lakes with a subsequent selection of lineages adapted to the cur-
rent environment or in situ radiation, which has been explored for
diatoms in isolated ecosystems (Stelbrink et al., 2018). A significant
(after Bonferroni correction) clustering signal in space as well as
through time is also most obvious for Staurosira, supporting its af-
finity to diversify along the ecological gradient of the Siberian tree
line (Stoof-Leichsenring et al., 2015). Diversification in Staurosira
and related genera (Staurosirella and Pseudostaurosira) is also detect-
able in the variety of present morphotypes reported from lakes of
the Siberian tree line area (Stoof-Leichsenring et al., 2014) and also
from other regions in the Circum-Arc tic (Paull, Hamilton, Gajewski, &
LeBlanc, 20 08) and North Amerika and Mongolia (Morales, Edlund,
& Spaulding, 2010).
Interestingly, all other genera with more distantly related lin-
eages present less pronounced environmental filtering and show
only few significant deviations from randomized null communities,
indicating mostly random community assemblages in the investi-
gated lakes across the tree line ecotone. Core samples of dif ferent
time slices and dif ferent past vegetation periods produced mostly
clustering signals (predominantly in Staurosira) or random patterns,
and only a few samples, with weak statistical support, indicated
over-dispersed or even communities.
Nearest taxon index and NRI values are known to reflect slightly
different results: NTI is more suitable for detec ting patterns based
on competition, whereas NRI is more efficient in detecting patterns
of environmental filtering (Kraft, Cornwell, Webb, & Ackerly, 20 07).
Furthermore, it has been suggested that richness of sequence types
in the sample compared with richness in the species pool can bias
NTI and NRI values, promoting the effects of environmental filtering
in a large species pool (Kraft et al., 2007). These biases could have
also affected our results, as Staurosira, Aulacoseira and Stauroneis
show highest richness among all genera analysed and calculated in-
dices are mostly related to environmental filtering.
4.3 | Relationship between
taxonomic and phylogenetic diatom turnover and
environmental change
In our study, distance-based redundancy analyses based on t axonomic
and phylogenetic composition support the assembly of main diatom
genera (Aulacoseira, Pinnularia, Sellaphora, Stauroneis and Staurosira)
being majorly explained by HCO3
− concentrations, water depth and
geography. Morphological diatom data have demonstrated that the
overall diatom variance in Siberian lakes sampled from Arctic to bo-
real environments is mostly explained by conduc tivit y, lake vegeta-
tion ty pe and me an July air temp era tu re, whe rea s si lic a, pH and wat er
depth explain less variance (Pestryakova, Herzschuh, Gorodnichev,
−2
0
2
4
0
20
40
60
80
surface samples
relatedness indices
NRI and NTI from surface samples (Sellaphora)
even/over-dispersed
communities
phylogenetically clustered
communities
type
NRI
NTI
significance
n.s.
p < 0.05
p = 0.001
(g)
TUNDRAFOREST-TUNDRAFOREST
−1
0
1
relatedness indices
NRI and NTI from core samples (Sellaphora)
even/over-dispersed
communities
phylogenetically clustered
communities
type
NRI
NTI
significance
n.s.
p < 0.05
p = 0.001
present 600 900 1800 2300 3800 5500 6100 6600 6900
(h)
TUNDRA FOREST-TUNDRA FOREST
sample age in cal yr BP
−4
−2
0
2
0
20
40
60
80
surface samples
relatedness indices
NRI and NTI from surface samples (Stauroneis)
even/over-
dispersed
communities
phylogenetically clustered
communities
(i)
type
NRI
NTI
significance
n.s.
p < 0.05
p = 0.001
TUNDRAFOREST-TUNDRA FOREST
−2
−1
0
1
relatedness indices
NRI and NTI from core samples (Stauroneis)
TUNDRA FOREST-TUNDRAFOREST
(j)
sample age in cal yr BP
present 600 900 1800 2300 38005500 6100 6600 6900
type
NRI
NTI
significance
n.s.
p < 0.05
p = 0.001
even/over-dispersed
communities
phylogenetically clustered
communities
FIGURE 5 Continued
|
11
STOOF-LEI CHSENR ING ET aL .
& Wetterich, 2018). It has been hypothesized that there is a strong
interaction between lake vegetation type and conductivity, which is
mainly driven by HCO3
− concentrations, explaining increased HCO3
−
concentrations in boreal lakes compared to tundra lakes (Herzschuh
et al., 2013). Likewise, our data support that HCO3
− mainly explains
diatom variance in the genera Staurosira, Pinnularia, Sellaphora and
Stauroneis, except Aulacoseira is largel y explained by spatial variable s.
Because HCO3
− concentrations and spatial variables partly mirror
vegetational changes across the sampled ecotone, we assume that
additional environmental variables, such as vegetation type or related
environmental variables that have not been exclusively considered in
this study, co nt rib ut e to the diatom com mu nit y assem bly. Geogra phic
distance, however, seems to be of weaker influence, this has been
shown in other alpine and boreal studies (Feret, Bouchez, & Rimet,
2017; Teitt inen & Soin inen, 2015) an d has been de mo ns tr ated fo r the
genus Staurosira across a similar area (Stoof-Leichsenring et al., 2015)
and for this study as well.
Until recently, it is still unclear whether diatoms can gener-
ally adapt to recent global climate change (Ir win, Finkel, Müller-
Karger, & Troccoli Ghinaglia, 2015) and if vegetation changes,
which already resulted in the greening and browning of the tun-
dra (Fu, Su, Wang, & Sui, 2019; Lara, Nitze, Grosse, Martin, &
McGuire, 2018), will eventually cause the disappearance of spe-
cific diatoms along with the potential loss of the tundra biome
in the future. Furthermore, temperature-related variables, like
ice cover duration, thermal stratification (Rühland, Priesnit z, &
Smol, 2003), primary production (Drake et al., 2019) and nutri-
ent availability in Arctic lakes (Pestryakova et al., 2018) are af-
fected by recent global warming. Lacking thermal stratification
and nutrient increase (Sienkiewic z, Gąsiorowski, & Migała, 2017)
as well as the lengthening of the growing season (Smol et al.,
2005) resulted in drastic replacements of established diatom as-
semblages. Especially, the reduction in ice cover duration altered
the abundance of diatoms of the genus Fragilaria (synonymous
for Staurosira; Keatley, Douglas, & Smol, 2008; Smol & Douglas,
2007; S mol et al., 20 05;). In contr ast , growth experiments on ma-
rine diatoms suggest adaptation to rapidly increasing temperature
is possible (Jin & Agustí, 2018; O'Donnell et al., 2018), whereas
other studies also identify a loss of diversity in cold-adapted di-
atoms (Lazarus, Barron, Renaudie, Diver, & Turke, 2014). From
our data, however, we can conclude that for taxonomically and
phylogenetically poor genera (Ellerbeckia, Urosolenia, etc.), envi-
ronmental change will putatively result quickly in the absence of
lineages. In contrast, lineages of taxonomically highly diverse and
phylogenetically less differentiated diatom genera (Staurosira and
Aulacoseira) have greater capabilities to adapt to environmental
changes by shifting their abundancies without being entirely
lost. Lineages of genera, which are less taxonomically diverse
but largely phylogenetically differentiated (Nitzschia, Pinnularia,
Sellaphora and Stauroneis) will putativel y sh if t in abu ndanc e, b een
replaced or lost. This is likely because they can poorly cope with
environmental changes as they are strongly adapted to specific
environmental conditions.
TABLE 2 Result s of the dbRDA analyses of the 19 diatom genera datasets obtained from the lake surface samples
Genera
Taxonomic beta diversity Phylogenetic beta diversity Mantel test
Selected variables R2
R2
adj pSelected variables R2
R2
adj p R p
Staurosira HCO3
− + dep + PCNM1 0. 261 0. 231 .001*** HCO3
− + dep 0.110 0.086 .0 01*** 0.254 .001***
Aulacoseira PCNM1 + dep + PCNM7 + PCNM10
+ PCNM9
0.054 0.054 .001*** PCNM1 + dep + PCNM9 0.245 0.213 .001*** 0.439 .001***
Pinnularia HCO3
− + PCNM11 + PCNM9 + PCNM4 0.082 0.032 .002** dep + PCNM11 + HCO3
−0.081 0.044 .001*** 0.492 .001***
Sellaphora PCNM1 + dep + PCNM2 + HCO3
− + P
CNM4
0.124 0.062 .001*** PCNM4 + PCNM2 + dep 0.102 0.066 .001*** 0.431 .001***
Stauroneis dep + HCO3
−0.058 0.033 .001*** PCNM5 + pH 0.127 0.103 .00 4** 0. 452 .001***
Note: Variables for dbRDA were selected with the function ordistep, only pre-selec ted variables were included in the dbRDA. Mantel test compared distance matrices derived from taxonomic and
phylogenetic beta diversity per genus.
p values are coded in ***0.0 01, **0.01, *0.05, •0.1; HCO3
−, Hydrogen carbonate; dep, lake water dept h; pH, pH value; PCNM eigenvec tors indicate spatial variables.
12
|
STOOF-LEICHSENR ING ET aL .
5 | CONCLUSION
In general, our study supports using environmental DNA from lake
sediment archives to infer taxonomic and phylogenetic diversity
directly through time and space, thereby allowing a deeper un-
derstanding of assembly rules by combining recent and temporal
patterns of communit y assemblage in minute eukaryotic algae. In
particular, our study reveals that lake environmental conditions and
phylogenetic diversity, which is a result of evolutionary differentia-
tion, are important factors in the assembly rules for diatom genera.
The sensitivit y of diatoms towards environment al change highlights
the importance of understanding the effec ts of climate variations on
arctic-boreal lake environments and community composition, espe-
cially under recent global climate change. Under the expectation that
phy logenetic diver si ty sh ap es the diatom assem bl y by affect ing rich-
ness and turnover in diatom genera, as shown for communities from
Siberian tree line lakes, we conclude that some diatom genera have
greater capabilities to adapt to environmental changes, whereas oth-
ers will be putatively replaced or lost due to the displacement of the
tundra biome and related changing environmental conditions.
ACKNOWLEDGEMENTS
We thank the Federal Ministry of Education and Research (BMBF,
grant no 5.2711.2017/4.6), the Russian Foundation for Basic
Research (RFBR, grant no 18-45-140053 r_a) and the Project of the
North-Eastern Federal University (NEFU, Regulation SMK-P-1/2-
242-17 ver. 2.0, order no. 494-OD), which par tly financed the pro-
ject. In addition, we would like to acknowledge Alexey Pestr yakov
and his family for their great support during fieldwork, Evgenia
Mikhaylova (rector of NEFU) and the BIOM laboratory of NEFU.
DATA AVAILAB ILITY STATE MEN T
Raw sequence data, description of the bioinformatic filtering of the
raw sequence data and final tabular DNA sequence datasets are de-
posited in the Dryad Digital Repository (https ://doi.org/10.5061/
dryad.h1893 1zg9).
ORCID
Kathleen R. Stoof-Leichsenring https://orcid.
org/0000-0002-6609-3217
Laura S. Epp https://orcid.org/0000-0002-2230-9477
Ulrike Herzschuh https://orcid.org/0000-0003-0999-1261
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BIOSKETCH
Kathleen Stoof-Leichsenring is a group and laboratory leader of
the subresearch group of High Latitude Biodiversity in the sec tion
Environmental Terrestrial Systems at the Alfred Wegener Institute
Helmholtz Centre for Polar and Marine Biology (link to the web-
page: https ://www.awi.de/en/scien ce/geosc ience s/polar-terre
strial-envir onmen tal-syste ms/resea rch-foci/high-latit ude-biodi
versi ty.html). Her research interests are in palaeogenetic and pal-
aeoenvironmental research with a focus on diatom diversity and
their evolutionar y patterns in space and through time.
Author contributions: K. S-L. and U.H. designed research; K.S-L.,
U.H and L.P. performed field sampling; K.S-L. and U.H performed
research, while L.E. performed core sediment subsampling and
K. S-L. per fo rmed ge netic laborato ry work; K.S -L and U.H ana lysed
data; K.S-L. wrote the article that all co-authors commented on.
SUPPORTING INFORMATION
Additional supporting information may be found online in the
Suppor ting Information section.
How to cite this article: Stoof-Leichsenring KR, Pestr yakova
LA, Epp LS, Herzschuh U. Phylogenetic diversity and
environment form assembly rules for Arctic diatom
genera—A study on recent and ancient sedimentary DNA. J
Biogeogr. 2020;00:1–14. htt ps ://doi.or g/10.1111/jb i.13786
